Phytomanagement of Metal(loid)-Contaminated Soils: Options, Efficiency and Value
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REVIEW
published: 04 August 2021
doi: 10.3389/fenvs.2021.661423
Phytomanagement of
Metal(loid)-Contaminated Soils:
Options, Efficiency and Value
Helena Moreira 1*, Sofia I. A. Pereira 1, Michel Mench 2, Carlos Garbisu 3, Petra Kidd 4† and
Paula M. L. Castro 1
1
Universidade Católica Portuguesa, CBQF—Centro de Biotecnologia e Química Fina – Laboratório Associado, Escola Superior
de Biotecnologia, Porto, Portugal, 2Univ. Bordeaux, INRAE, BIOGECO, Pessac, France, 3Department of Conservation of Natural
Resources, NEIKER-Basque Institute for Agricultural Research and Development, Basque Research and Technology Alliance
(BRTA), Derio, Spain, 4Instituto de Investigacións Agrobiolóxicas de Galicia (IIAG), Consejo Superior de Investigaciones Científicas
(CSIC), Santiago de Compostela, Spain
The growing loss of soil functionality due to contamination by metal(loid)s, alone or in
combination with organic pollutants, is a global environmental issue that entails major risks
to ecosystems and human health. Consequently, the management and restructuring of large
Edited by: metal(loid)-polluted areas through sustainable nature-based solutions is currently a priority in
Jane A Entwistle,
Northumbria University, research programs and legislation worldwide. Over the last few years, phytomanagement has
United Kingdom emerged as a promising phytotechnology, focused on the use of plants and associated
Reviewed by: microorganisms, together with ad hoc site management practices, for an economically viable
Richard Alastair Lord,
and ecologically sustainable recovery of contaminated sites. It promotes simultaneously the
University of Strathclyde,
United Kingdom recovery of soil ecological functions and the decrease of pollutant linkages, while providing
Andrew Brian Cundy, economic revenues, e.g. by producing non-food crops for biomass-processing technologies
University of Southampton,
United Kingdom (biofuel and bioenergy sector, ecomaterials, biosourced-chemistry, etc.), thus contributing to
*Correspondence: the international demand for sustainable and renewable sources of energy and raw materials for
Helena Moreira the bioeconomy. Potential environmental benefits also include the provision of valuable
hgmoreira@ucp.pt
ecosystem services such as water drainage management, soil erosion deterrence, C
†
Deceased
sequestration, regulation of nutrient cycles, xenobiotic biodegradation, and metal(loid)
stabilization. Phytomanagement relies on the proper selection of (i) plants and (ii) microbial
Specialty section:
This article was submitted to inoculants with the capacity to behave as powerful plant allies, e.g., PGPB: plant growth-
Toxicology, Pollution and promoting bacteria and AMF: arbuscular mycorrhizal fungi. This review gives an up-to-date
the Environment,
a section of the journal overview of the main annual, perennial, and woody crops, as well as the most adequate
Frontiers in Environmental Science cropping systems, presently used to phytomanage metal(loid)-contaminated soils, and the
Received: 30 January 2021 relevant products and ecosystems services provided by the various phytomanagement
Accepted: 21 June 2021
options. Suitable bioaugmentation practices with PGPB and AMF are also discussed.
Published: 04 August 2021
Furthermore, we identify the potential interest of phytomanagement for stakeholders and
Citation:
Moreira H, Pereira SIA, Mench M, end-users and highlight future opportunities boosted by an effective engagement between
Garbisu C, Kidd P and Castro PML environmental protection and economic development. We conclude by presenting the legal
(2021) Phytomanagement of
Metal(loid)-Contaminated Soils: and regulatory framework of soil remediation and by discussing prospects for
Options, Efficiency and Value. phytotechnologies applications in the future.
Front. Environ. Sci. 9:661423.
doi: 10.3389/fenvs.2021.661423 Keywords: phytoremediation, cash crops, cropping systems, PGPB, bioeconomy, bioinoculants, AMF
Frontiers in Environmental Science | www.frontiersin.org 1 August 2021 | Volume 9 | Article 661423
Moreira et al. Phytomanagement of Metal(loid)-Contaminated Soils
INTRODUCTION methodologies (Kidd et al., 2015). Amongst these,
phytotechnologies stand out as a cost-effective, sustainable
Soil contamination with metal(loid)s, termed also ‘trace elements’ option for the recovery of TE-contaminated areas (Mench
in Biogeochemistry and Life Sciences (hereafter referred as TE) is et al., 2010, 2018; Herzig et al., 2014; Thijs et al., 2018; Kolbas
a global environmental issue that poses serious risks for et al., 2020). Phytotechnologies involve a set of techniques that
ecosystem integrity and human health (Joimel et al., 2016; exploit plants and sustainably manage “soil-plant-microbial”
Hou et al., 2017; Pérez and Eugenio, 2018; Bagherifam et al., systems to recover polluted sites, especially those with low and
2019; Mench et al., 2020; Haller and Jonsson, 2020). Although medium levels of soil pollution (Vangronsveld et al., 2009; Mench
background and bioavailable TE levels are generally low in soils, et al., 2010, 2018). Regarding TE-pollution, phytotechnologies
except at geochemical anomalies with either deficiency or can also be an effective choice for highly contaminated sites when
exceedance, anthropogenic activities such as industry, mining, the goal is stripping the soil of its bioavailable metal(loid)
smelting and metallurgy, intensive agriculture, e-wastes, traffic, fractions, or TE-stabilization (thus, decreasing potential TE
use of fossil fuels, etc. have caused an increase in soil TE toxicity). This can be tackled through TE uptake and
concentrations reaching hazardous levels (Alloway, 2013; accumulation in harvestable plant parts (e.g., phytoextraction),
Kumpiene et al., 2017; Petruzzelli et al., 2020). Furthermore, or by progressively promoting in situ inactivation by combining
anthropogenically-released TE tend to have higher availability the use of TE-excluding plants, soil amendments and/or
and mobility than those resulting from natural processes (Kabata- microbial inoculants (assisted phytostabilization), respectively
Pendias, 2010), raising environmental and human health (Mench et al., 2010, 2018; Epelde et al., 2014; Kidd et al.,
concerns. In the European Union (EU), there are at least 2.8 2015; Burges et al., 2016, 2017, 2018). Phytoextraction options
million potential contaminated sites and 650,000 registered sites can also be assisted by soil amendments, chemical agents and soil
where polluting activities occurred or are occurring (Pérez and microorganisms (assisted phytoextraction) (Vangronsveld et al.,
Eugenio, 2018). Such high number of contaminated sites, coupled 2009; Mench et al., 2010; Kidd et al., 2015; Wang et al., 2019;
with the threat posed by contaminants to environmental and Kolbas et al., 2020). Within this context, microbial bioinoculants
public health, pushed policymakers and legislators to 1) set soil and site-tailored cropping systems are most useful tools to help
protection as a strategic priority and 2) encourage the plants cope with soil contamination. Not surprisingly, the
remediation, reclamation, restoration and recovery of those research on microbial bioinoculants (e.g., plant growth-
sites (Reinikainen et al., 2016; Castelo-Grande et al., 2018; promoting bacteria - PGPB and arbuscular mycorrhizal fungi -
Ramon and Lull, 2019). Consequently, nowadays, numerous AMF), soil amendments (organic and/or inorganic), and suitable
countries have specific legislation and guidelines to deal with cropping patterns (e.g., intercropping, winter cropping) escalated
contaminated sites and are committed to their remediation, based in the last decade, yielding very positive and encouraging
on either regulatory values or site-specific risk assessment, which outcomes.
further depends on contemplated future land use (Mench et al., In the recent past, phytotechnologies were combined with
2020). This has boosted the number of initiatives in the EU aimed sustainable site management practices, giving birth to a wider
at recovering contaminated sites (Pérez and Eugenio, 2018). approach—phytomanagement—where environmental benefits
However, despite this positive trend, these numbers fall short are allied with financial returns for stakeholders, and/or wider
given the extent of the problem. social and economic benefits to the surrounding community
The recovery of TE-polluted land is critical to enhance soil (Robinson et al., 2009; Cundy et al., 2016; Burges et al., 2018;
ecosystem services, as well as to decrease the contamination of the Li et al., 2018; Bardos et al., 2020). Beside presenting a plethora of
soil matrix itself, together with that of recipient waterbodies and ecological benefits such as the progressive reestablishment of soil
food crops, thus ensuring human welfare. Additionally, the health and decreased TE run-off risks, phytomanagement places
reclamation of contaminated sites through phytomanagement emphasis on obtaining economic profits by using cash crops to
creates a set of opportunities to comply with the net-zero carbon produce biomass for renewable energy and valuable materials
emissions targets, by generating areas that act as carbon sinks and (Evangelou et al., 2015; Kidd et al., 2015; Cundy et al., 2016; Šimek
by implementing programs for valuing land that commensurate et al., 2017; Thijs et al., 2018; Xue et al., 2018). Phytomanagement
with the current sustainability paradigm (Bardos et al., 2016, is in line with the objectives of the European Green Deal roadmap
2020; Cundy et al., 2021). Furthermore, the use of contaminated that aims at turning climate and environmental challenges into
lands for bioenergy production can importantly reduce the opportunities, restoring biodiversity and decreasing pollution.
clearing of agricultural/fertile areas for this purpose, leading to Using contaminated sites, for instance, for bioenergy production
greenhouse gas emission savings (Mellor et al., 2021). In the last supports the growing demand for energy sources alternative to
years, stakeholders, including site owners, local population, fossil fuels, while reducing the prevailing pressure on the use of
investors and public authorities, are increasing their forests or agricultural productive land for the productions of
environmental awareness and gradually recognizing that biofuels (Edrisi and Abhilash, 2016; Sytar and Prasad, 2016).
recovered sites can provide values, goods and services, and Under this scope, this review aims to: 1) provide an overview
then demanding the management and recovery of of the main traits and potential economic applications of the most
contaminated land. In the last 2 decades, environmentally- widely used TE-tolerant cash crops that better fit
friendlier, greener technologies have paved the way to become phytomanagement goals; 2) summarize selected field
reliable alternatives to previously favored disruptive phytomanagement experiments (especially those published in
Frontiers in Environmental Science | www.frontiersin.org 2 August 2021 | Volume 9 | Article 661423Moreira et al. Phytomanagement of Metal(loid)-Contaminated Soils
2010–2020) using these plants; 3) indicate suitable crops that can ashes used as ecocatalysts in biosourced fine chemistry (Clavé
be coupled with cash crops to improve site management and et al., 2016; Quintela-Sabarís et al., 2017; Mench et al., 2018; Xue
phytomanagement effectiveness; 4) address the importance of et al., 2018; Bihanic et al., 2020; Kolbas et al., 2020). The
cropping patterns and the use of amendments in the remediation production of high-value products fits the Circular Economy
of TE-contaminated sites; and 5) explore the use of (CE) and Bioeconomy paradigms, both highly promoted within
microorganisms, namely PGPB and AMF, as probiotics for the EU and other strong economies such as China,
soil health recovery and plant performance (establishment, United Kingdom, Canada and Japan (Korhonen et al., 2018).
survival, growth, and physiological traits). Cash crops were The CE paradigm promotes economic development through a
selected based on their ability to provide suficient harvestable cyclical flow of materials that spill over as direct and indirect
biomass that can be processed, especially for the local benefits to the environmental and social dimension of our society
bioeconomy, and of which there is a significant body of (Korhonen et al., 2018). However, CE requires a shift in the
literature based on empirical research, especially from field society´s mindset and requires, among other aspects, the design
trials. We conclude by highlighting the current status of of new business models and robust networking and innovation in
phytomanagement and the legal and regulatory frameworks production processes and commercial products (Prieto-Sandoval
for its implementation across Europe. et al., 2018).
The type of amendments, cropping systems and their Regarding the potential environmental benefits, at the local
combination provides a myriad of possible scenarios. This level, phytomanagement improves soil health and fertility (Herzig
topic is a matter of thorough scrutiny elsewhere (e.g., Kidd et al., 2014; Kidd et al., 2015; Touceda-González et al., 2017; Xue
et al., 2015), and therefore it will not be exhaustively et al., 2018), soil organic matter (OM) quantity and quality
addressed here. Genetic-engineered cultivars are also beyond (Mench et al., 2018; Risueño et al., 2020; Álvarez-Rogel et al.,
the scope of this review (for information on this topic, see for 2021) and soil biodiversity, both faunal (Chauvat et al., 2014) and
instance Gunarathne et al., 2019 and Sebastian et al., 2019). microbial (Foulon et al., 2016; Šimek et al., 2017; Durand et al.,
2018; Xue et al., 2018; Garbisu et al., 2020; Kidd et al., 2021). At
the large scale, phytomanagement can enhance carbon
PHYTOMANAGEMENT BENEFITS AND sequestration, mitigate the emission of greenhouse gases, and
CONSTRAINTS—BRIEF OVERVIEW reduce and/or prevent TE dispersion (Evangelou et al., 2012a;
Kidd et al., 2015; Cundy et al., 2016; Šimek et al., 2017; Xue et al.,
Soil contamination reduces site’s economic, ecological and social 2018).
values. As addressed, a suitable and cost-effective option to As a risk-based approach, prior to its implementation,
remediate such contaminated sites and restore land values is phytomanagement requires an initial risk assessment to
the phytomanagement, a multi-objective management strategy evaluate pollutant linkages (source-pathway-receptor)
that reconciles economic and social returns with ecological gains (Figure 1) (Cundy et al., 2016; Reinikainen et al., 2016). Upon
(Figure 1) (Nsanganwimana et al., 2014; Kidd et al., 2015; Burges this risk evaluation, an option appraisal must be conducted by
et al., 2018). Phytomanagement can provide financial benefits weighting several variables such as feasibility, time, economic
through planting valuable crops that serve as feedstock for viability, legal requirements, social approval, etc. to properly
multiple industries and end-products such as furniture, pulp outline the best way of handling the abovementioned pollutant
and paper, biochemicals (adhesives and detergents), insulation linkages. Option appraisal is a baseline cornerstone for the
and building materials, composites and plastic alternatives, food successful design of any restoration plan (Mench et al., 2020).
additives, animal feeding and bedding, etc. Some of these crops In addition, for phytomanagement to be fully operational at a
can also be used as bioenergy crops yielding high-quality biomass given site, an optimization stage before full-scale implementation
(Nsanganwimana et al., 2014, 2015; Burges et al., 2018; Lacalle is required. At this stage, issues related to edaphoclimatic
et al., 2018; Mench et al., 2018; Thijs et al., 2018) to produce conditions are addressed to guide the selection of the most
renewable energy (electricity, heat and biofuels) (Gonsalvesh appropriate crops. Potential edaphic constrains typically
et al., 2016; Pandey et al., 2016; Rizwan et al., 2018; Grottola include physical and chemical characteristics of the soil.
et al., 2019; Pogrzeba et al., 2019; Rusinowski et al., 2019; Sidhu Physical constrains typically regard to compaction, reduced
et al., 2020; Tran et al., 2020 ). Most importantly, these crops offer water holding capacity and low aeration (Shrestha and Lal,
the possibility to combine the production of biomass for energy 2011), whereas chemical properties are usually related to low
production and/or other end-products (Grisan et al., 2016; Barla (or high) pH, high TE concentrations, mixtures of TE with other
and Kumar, 2019) with TE phytoextraction or phytostabilization pollutants (e.g., mineral oils, polycyclic aromatic hydrocarbons,
(Thijs et al., 2018; Chalot et al., 2020). Likewise, they can pesticides, polychlorinated biphenyls, organochlorines, per- and
simultaneously promote the biodegradation of soil organic polyfluoroalkyl substances), low nutrient and OM contents, etc.
contaminants. Economic revenues can also be obtained (Kidd et al., 2015). These soil characteristics depend on ongoing
through phytomining, a phytotechnology focused on the and/or past polluting activities, which in the case of industrial
recovery of valuable TE (e.g., Co, Ni, and Re) from the TE- contaminated sites depend on the type of industry and its
rich biomass of hyperaccumulators (also called bio-ores) products (Alloway, 2013). The effects of high TE
(Remigio et al., 2020; Chaney et al., 2018). TE-rich phytomass concentrations depend on their intricate reactions with soil
can be pyrolysed/calcinated and the resulting biochar and/or phases, namely through, e.g., dissolution, sorption,
Frontiers in Environmental Science | www.frontiersin.org 3 August 2021 | Volume 9 | Article 661423Moreira et al. Phytomanagement of Metal(loid)-Contaminated Soils FIGURE 1 | Phytomanagement of TE-contaminated soils: challenge, strategy and impacts. Frontiers in Environmental Science | www.frontiersin.org 4 August 2021 | Volume 9 | Article 661423
Moreira et al. Phytomanagement of Metal(loid)-Contaminated Soils complexion, precipitation, which are a function of soil properties contents, leading to a higher production rate of bioethanol (Kabata-Pendias, 2010). For instance, a soil with low pH can (Geiger et al., 2019). increase the ion species of some TE (e.g., metallic cations) Metal(loid)-enriched biomass can be processed by torrefaction dissolved in soil solution, rendering them more bioavailable and pyrolysis for producing biofuels and tars (Bert et al., 2017). (Young, 2013). Similarly, climatic conditions also pose critical Accordingly, the potential emission of volatile TE chemicals at limitations to phytomanagement success. Temperature shapes high pyrolysis temperatures, the potential leaching of minerals plant transpiration, growth and metabolism, as well as water and organics from chars, and the product quality of the products chemistry, thus directly affecting both contaminant uptake and deserve attention. The TE fate depends on complex and its fate in plant parts and other ecosystem compartments multifactorial processes for all technologies based on thermal (Bhargava et al., 2012). Likewise, moisture affects plant conversion (e.g., incineration, pyro-gasification, and pyrolysis) growth, faunal and microbial activity, and contaminant (Edgar et al., 2021). Oxide-forming elements and refractory transport within soil. Prolonged drought induces plant stress, compounds are often found in ashes and tars. Capture of enhancing plant sensitivity to pathogens and herbivory and, volatile Cd and As chemicals depends on the filter quality. notably, reducing plant growth (Kidd et al., 2015). Hence, Ecocatalysts prepared from hyperaccumulators are used in water management needs to be carefully considered, especially various ways but preparing them with the most essential in arid and semi-arid areas that undergo relatively long periods of elements (e.g., Zn, Cu, Co, and Mn) and the least non- drought and/or heatwaves, and soils with low water holding essential elements (Cd, As) requires a strong selection of plant capacity (Kidd et al., 2015). Therefore, only plants that species (Clavé et al., 2016). Besides the energy sector (e.g., successfully withstand all these conditions can be used to bioethanol, biodiesel, biogas, and heat), many chemical, phytomanage a contaminated site, especially in the current physical and biological biomass-processing technologies are scenario of climate change. In addition, under such reported as pre-treatment and conversion technologies. In the conditions, the selected crops need to achieve case of anaerobic digestion, some TE excess (e.g., economically-viable yields and their products should be >500 mg Zn kg−1, 20,000 mg Mn kg−1) can decrease the non-potentially toxic and fit to the quality standards. A methane content in biogas and daily methane production large proportion of the aboveground biomass harvested at (Edgar et al., 2021). Essential oils from aromatic plants phytomanaged sites is from meta(loid)-excluders and harvested at phytomanaged sites also did not show TE therefore free of metal(loid)s excess. Also, root-to-shoot contamination (Raveau et al., 2020). Similarly, oilseeds from transfer of organic contaminants is frequently low, except sunflower, hemp, and most Brassicaceae harvested at for some xenobiotics such as organochlorines. Conversely, phytomanaged sites generally do not present TE excess, nor some elements (e.g., Ca, Si, Mg, etc.), as well as biomass the oil for biodiesel production and other uses. moisture, may be of concern for the energy sector Several pre-treatments can separate the metal(loid)s from (Nsanganwimana et al., 2013; Nsanganwimana et al., 2014). the biomass fraction of interest or on the contrary avoids their Regarding combustion and pyrolysis, both intrinsic alkali release during the process and limit their bioavailability in the metals (e.g., K and Ca) and silica present in the material biochars produced (Edgar et al., 2021): pre-mixing with (which can react to form alkali silicates), and contamination chemicals (e.g., MgCO3, FeCl3 and Fe(NO3)3, CaO) before of the harvested biomass by soil, may induce operational biomass pyrolysis (He et al., 2020); composting (except the problems such as ‘slag’ formation. In particular, for some methylation of Hg-chemicals); for anaerobic digestion and crops, such as Miscanthus x giganteus and Arundo donax, a fermentation, pre-treatment with NaOH enhances the delayed harvest can reduce undesirable components (K, Ca, P, release of biogas and metals from straw; biomass S, and N) in the biomass. pretreatments with either ethanol organosolv, soda or dilute According to some studies, TE excess in the biomass can acid (Asad et al., 2017) and steam explosion (Ziegler-Devin induce changes in heavy hydrocarbons present in tars, bio-oil et al., 2019) to release TE before bioethanol production. Post- yield, ash content, and relative evolution of CO2 and H 2 in treatment of conversion products and platform chemicals is volatiles (reduced CO content) (Edgar et al., 2021). For also an option (e.g., sorption of arsenicals by Fe hydroxides poplar and willow short rotation coppice (SRC), Zn and after solvolysis of Pteris vittata fronds (Carrier et al., 2011). Cd concentrations are higher in bark than in wood, Overall, selection of plant species and cultivars, agricultural decreasing in older branches and trunk. In addition, foliar practices, harvest timing, etc., can also improve the quality of Zn and Cd concentrations can decrease with growth and the harvested biomass compared to the required standards of successive cuts. Therefore, the selection of the harvested the biomass-processing technologies. shoot parts and their age are an important factor (Grignet Phytomanagement of TE-contaminated sites is certainly et al., 2020; Grzegórska et al., 2020). Trees growing at expanding (Pérez and Eugenio, 2018), but it is still rarely brownfield and landfill sites can exhibit higher lignin chosen as a remediation technology when compared to content than those cultivated in uncontaminated soils due conventional physicochemical methods of soil remediation to abiotic stresses, e.g., drought-stress, leading to lower (Kidd et al., 2015; Quintela-Sabarís et al., 2017). As a matter glucose yield (Edgar et al., 2021). In contrast, vetiver of fact, once a contaminated site is targeted for recovery, the most plants exposed to Cu excess can display a decrease in typical procedure is to engage in faster and more drastic solutions, lignin and an increase in hemicellulose and cellulose generally involving the use of physicochemical techniques (e.g., Frontiers in Environmental Science | www.frontiersin.org 5 August 2021 | Volume 9 | Article 661423
Moreira et al. Phytomanagement of Metal(loid)-Contaminated Soils
soil replacement and soil washing) and civil engineering works trees), water requirements, root depth, susceptibility to diseases/
(Ashraf et al., 2019), which often remove the target pollutants at pests, etc. must be taken into account (Kidd et al., 2015). Also,
the expense of the destruction of soil integrity and functionality. the potential for volatilization (Hg and Se) (Ali et al., 2013)
This is, at least partly, due to technical issues related to the should be carefully anticipated. Importantly, for TE
implementation of phyto-based strategies, as well as to the phytostabilization, plants should contain low levels of TE in
perception of many stakeholders who have a low confidence the harvestable biomass (unlike for phytomining and
on the reliability of phytotechnologies (Cundy et al., 2013, 2015; bioavailable contaminant stripping). In any case, TE uptake
Reinikainen et al., 2016; Ramon and Lull, 2019). Contributing to and accumulation are TE- and host-specific, can be highly
this is the lack of 1) convincing pilot field applications of plant- variable within plant species and their populations (different
based options and 2) specific legal frameworks (Cundy et al., variants or cultivars) (Ruttens et al., 2011), and depends on site
2016). In any event, phytomanagement can also be handled as a specificities. Plants should also be resilient to other abiotic
holding-strategy for unused and vacant contaminated sites factors often related with contaminated areas, which can
(Moreira et al., 2021). include soil nutrient deficiencies, salinity, compaction, etc.
In summary, environmental and socioeconomic benefits of (Kidd et al., 2015).
phytomanagement options largely depend on specific site For TE-contaminated sites, local colonizing florae,
requirements, such as the need for amendments and irrigation, described as metallophytes (endemic plants found in TE-
specific agronomic techniques, maintenance costs, presence of rich soils) and pseudo-metallophytes (facultative
biomass processing units nearby to decrease costs, etc. Economic metallophytes, i.e., plants with abilities to grow in both TE
benefits obtained from harvested biomass and from other and non TE-rich soils) (Favas et al., 2014), should be firstly
potential end-products can be easily valued, but social and considered. They present specific traits resulting from the
environmental benefits (e.g., ecosystem services) are much adaption to local harsh conditions that grant them
more difficult to calculate (Bardos et al., 2016; Kuppens et al., advantages in plant establishment and growth. Furthermore,
2018). In any case, different sites with different contamination the use of local colonizing florae prevents ecological site-
histories frequently require different technologies for their disturbances that potentially invasive/aggressive species may
remediation and recovery, for achieving the desirable goals trigger, by competing with local species and/or acting as
and end-uses. ecological disruptors. For instance, Jatropha curcas L., a TE-
tolerant bioenergy crop is native in Mexico but in some
countries, such as Indonesia, Australia and South Africa, is
PLANT SELECTION registered as invasive. This issue can be attenuated by using
sterile cultivars, if available, to avoid further colonization,
Phytomanagement uses plants that can withstand moderate or although propagation by stem cuttings is more difficult to
high bioavailable levels of TE (and of organic compounds), as prevent. The use of metallophytes in phytomanagement is
well as other abiotic stresses while offering financial returns and usually thwarted by their typical low biomass, slow-growing
environmental gains. The selection of the most suitable plant nature and reduced economic value for stakeholders, except
species for a contaminated site is therefore a critical point and when used for phytomining (e.g., Ni by Allyssum species)
depends on several factors, namely: 1) type, concentration, (Chaney et al., 2007; Remigio et al., 2020). However, they
chemical speciation, bioavailability and location of soil could still be used, for example, as cover crops, intercrops and
contaminants; 2) physicochemical soil properties (e.g., plant borders in phytomanagement initiatives. Conversely,
structure, compaction, fertility, moisture, pH, OM, etc.); 3) some pseudo-metallophytes fit the phytomanagement
water availability; and 4) climatic conditions (e.g., purposes by presenting high biomass and growth rate, while
temperature, precipitation, wind, and altitude) (O’Connor also overcoming constraints posed by abiotic and biotic
et al., 2019); and 5) combined life-cycles of pests and stresses.
biological auxiliaries. In particular, crops chosen for TE In the past 10–15 years, some energy crops have arisen as most
phytostabilization purposes should present a TE-excluder promising in adding value to TE-contaminated areas by
phenotype and avoid TE dispersion by leaching, water and generating biomass-based products (gaseous, liquid, and solid)
wind erosion (Mench et al., 2007; Ruttens et al., 2006a,b; (Grzegórska et al., 2020) that can be converted into different
Mench et al., 2010; Vangronsveld et al., 2009). Plants kinds of energy (heat, electricity, and fuel for transportation),
stabilize TE by root uptake and accumulation, precipitation while attaining environmental goals. Other industrial crops (e.g.,
and adsorption, and by changing their chemical form through fiber crops), aromatic plants, ornamental plants and
pH or redox potential modifications around roots (Mench et al., biofortified crops are also perfectly suitable for
2010; Burges et al., 2018; Yan et al., 2020). Conversely, plants phytomanagement, as one of the commitments of this
meant for TE phytoextraction translocate the TE from roots to phytotechnology is to deliver economic benefits for the end-
shoots and accumulate them in their aboveground tissues users (Gonsalvesh et al., 2016; Pandey et al., 2016; Rizwan et al.,
(Robinson et al., 2015; Remigio et al., 2020). 2018; Grottola et al., 2019; Sidhu et al., 2020).
Traits such as the level of TE tolerance, growth rate, crop Greenhouse and mesocosm experiments are often used to test
yield, type of life cycle (perennial, annual, and biennial), leaf promising plants and favorable clones and cultivars. Besides
habit (deciduous, evergreen), growth habit (grasses, shrubs, and traditional breeding, mutation and somatic embryogenesis
Frontiers in Environmental Science | www.frontiersin.org 6 August 2021 | Volume 9 | Article 661423Moreira et al. Phytomanagement of Metal(loid)-Contaminated Soils
TABLE 1 | Examples of field trials with economically valuable annual crops (sunflower, maize, tobacco).
Plant Species/Cultivars/ Site Duration TE concentration in Main results Suggested References
Clones/Hybrids soil (mg kg−1) uses for
plants
Sunflower n.p. Former waste 3 years Cr (39–141), Ni − ↑ TE concentration in roots, n.p. Kacálková
(Hellianthus incineration plant (23–122), Cd followed by leaves et al. (2014)
annuus L.) (Czech Republic) (1.6–6.8), − ↑ TF for Cd and Pb
Pb (44–193) − ↓ Cd and Pb concentrations
in grains
′Peredovick′ Uranium-mining- 34–170 days Cd (0.62), Co (23.8), − ↑ Growth up to 140 days (in Biomass for Kötschau
influenced area Cr (50.9), Cu (45.2), acidic soils) energy et al. (2014)
(Germany) Fe (42,700), Mn (989), − ↑ TE extraction over time
Ni (64.8), Pb (15.9), − BCF > 1 for Cd
Th (9.05), U (7.75), − BCF > 1 for all elements,
Zn (79.4) except for U when considering
the ratio with bioavailabe TE in
soil
Mutant line families Farmland near a 3 years Cd (3.9–4.6), − Similar DW over time for Biomass Thijs et al.
(resulting of chemical former Zn-smelter Zn (234), Pb (142) each mutant conversion (2018)
mutagenesis for TE (Belgium) − Distinct DW among mutants
tolerance of inbred − ↓ Aboveground yields
line IBL04) − BCF > 1 for Zn, BCF < 1 for
Pb for all mutants
− BCF > 1 or < 1 for Cd
depending on the mutant
− ↑ Zn extraction
− Pb < detection limit in seeds
40 oilseed cv. (e.g., Farmlands 126 days Cd (0.24/0.85) − ↑ Biomass of several cv. Edible oil Zehra et al.
′S-9178′) contaminated by − ↑ Grain yield in several cv. (2020a)
mining and other − Cd concentration ranked as
anthropogenic follows: shoots > seeds >
activities (China) roots
− TF > 1 in several cv.,
especially in acidic soils
− ↓ Cd content in oil
− ↑ Amount of oil in seeds of
some cv. (especially ′S-9178′)
with a very good amount of
oleic acid (55.6–77.1%) and
suitable for human
consumption
40 germplasms (e.g., Farmlands 126 days Pb (106.5) − ↑ Biomass of several cv. Edible oil Zehra et al.
′G.P:8585′) contaminated by − ↑ Pb content in plant tissues, Sunflower (2020b)
mining and other ranked as follows: shoots > meal
anthropogenic seeds > roots
activities (China) − TF > 1 in most cv.
− ↓ Pb content in oil
− Pb content of sunflower
meal under the legal limits
− ′G.P:8585′ coined as best
germplasm for restoring
moderately Pb-contaminated
sites, with oil’s Pb
concentration below Chinese
Food Safety Standards
Maize (Zea Z1-Z6 Area affected by 6 months Cd (5.4–8.9), − ↑ Biomass of some cv. Animal feed Meers et al.
mays L.) former smelters Zn (266–398), − ↓ TE concentration in grains (grain) (2010)
activities (Belgium) Pb (135–189) − ↑ Cd concentration in shoots Biogas
(over European standards for Digestate
maize fodder)
− ↓ Zn concentration in topsoil
(Continued on following page)
Frontiers in Environmental Science | www.frontiersin.org 7 August 2021 | Volume 9 | Article 661423Moreira et al. Phytomanagement of Metal(loid)-Contaminated Soils
TABLE 1 | (Continued) Examples of field trials with economically valuable annual crops (sunflower, maize, tobacco).
Plant Species/Cultivars/ Site Duration TE concentration in Main results Suggested References
Clones/Hybrids soil (mg kg−1) uses for
plants
CT38 and HZ (sweet Field contaminated 75 days Cd (1.4) − Regular growth Human feed Xu et al. (2013)
maize) with disposal of city − Cd concentrations ranked
wastes and batteries as follows: sheath > root >
(China) lamina > stem > grain
− ↓ Cd concentration in grain
(< China legal threshold for
human consumption)
Z1-Z7 (energy maize) Site affected by 5 months Cd (4.7–6.5), − ↑ DW variability among cv. Animal feed Van Slycken
former smelters Zn (210–339) − ↓ Cd and Zn concentrations (grain) et al. (2013b)
activities (Belgium) in plant tissues ranked as Biogas
follows: leaves > stem > grains
− Average total TE
concentrations in maize
cultivars of 0.96 ± 0.29 mg Cd
kg−1 and 219 ± 39 mg Zn kg−1
− Potential Cd and Zn
removal of 19 ± 6 g Cd ha-1 y-1
and 4.3 ± 0.9 kg Zn ha-1 y-1
n.p. Former waste 3 years Cr (39–141), − ↑ TE concentration in roots, n.p. Kacálková
incineration plant Ni (23–122), followed by leaves et al. (2014)
(Czech Republic) Cd (1.6–6.8), − ↑ TF of Cd and Pb
Pb (44–193) − ↓ Cr, Cd and Pb
concentrations in grains
′Bright Jean No. 7′ Pb-contaminated 1 year and Pb (5844) − ↑ Growth and biomass Animal feed Cheng et al.
agricultural area 11 months production (grain) (2015)
(Taiwan) − ↓ Pb concentrations in roots Thermal
and shoots over planting periods energy
− TF < 1
− ↑ BCF in roots followed by
leaves > stems > bracteal leafs
> cob > kernel
− ↓ Pb content in grain (< EU
legal threshold for animal feed)
19 cv. of southern Cd-contaminated n.p. Cd (1.64) − Cd accumulation in plant Human feed Wang et al.
China paddy field (China) tissues ranked as follows: (2016)
roots > shoots > grain
− DW, Cd accumulation and
grain yield varied according to
the cv.
− ↑ Cd in aboveground tissues
and high biomass of 2 cv.
− ↓ Cd in grains of 3 cv. (< EU
legal threshold for human
consumption)
n.p. Agricultural field 37 and 57 Cd (87) − ↑ Cd concentration n.p. Khaokaew
Tobacco (Thailand) days − TF > 1 and Landrot
(Nicotiana − ↑ BAF (2015)
tabacum L.) − ↑ Total Cd uptake from day
37 to day 57
− Hyperaccumulation values for
Cd (based on extractable TE)
′Virginia′ 3 contaminated sites 3 years Pb (4–116), − ↑ Pb and Cd concentration n.p. Zaprjanova
(Bulgaria) Cd (0.4–3), in leaves in sites with high et al. (2010)
Cu (15–399), concentration of these TE
Zn (35–280) − ↑ Cu concentration in leaves
− Zn concentration ranked as
follows: Leaves > blossoms >
roots > stems
′Virgina′ and ′Burley′ Mine tailings (Serbia) 3–4 months U (15.3) − ↑ Concentration in lower n.p. Stojanović
leaves than upper leaves et al. (2012)
− ↑ Accumulation in leaves
followed by stems
− Hyperaccumulation values
for U in both cv.
(Continued on following page)
Frontiers in Environmental Science | www.frontiersin.org 8 August 2021 | Volume 9 | Article 661423Moreira et al. Phytomanagement of Metal(loid)-Contaminated Soils
TABLE 1 | (Continued) Examples of field trials with economically valuable annual crops (sunflower, maize, tobacco).
Plant Species/Cultivars/ Site Duration TE concentration in Main results Suggested References
Clones/Hybrids soil (mg kg−1) uses for
plants
n.p. Two agricultural fields 60/80 days Cd (0.59/1.38) − ↑ BCF in lower leaves Animal feed Yang et al.
(China) − Cd concentrations in tissues (2017)
ranked as follows: Lower leaves
> middle leaves > upper leaves
> root > stalk (or > stalk > root)
Cd concentration in lower and
middle leaves after coppice
− Leaves DW: 4.24 tonne ha-1
to 5.03 tonne ha-1 and stalks
DW: 1.41 tonne ha-1 to 1.48
tonne ha-1
− Theoretical percentages of
extracted Cd: 132.06
/203.91 g ha-1
− Theoretical extraction
efficiency: 10%/6.7%
− ↓ Total and available Cd in
soil
Somaclonal tabacco Farmland 3 years Cd (3.9–4.6), Zn Variable biomass and TE Biomass Thijs et al.
variants (e.g., contaminated by Zn- (234), Pb (142) accumulation over the years conversion (2018)
′NBCu104′ and smelter fallout − Efficient Cd extraction
′NFCu719′) (Belgium) − BCF > 1 for Zn and Cd in
aerial parts
− BCF < 1 for Pb in aerial parts
Abbreviations are as follows: n.p., not provided; TF, Translocation factor; BCF, Bioconcentration factor; BAF, Bioaccumulation factor; DW, dry weight; cv., cultivar; ↑, high/higher/increase;
↓, low/lower/decrease.
Values for TE concentrations are given for the upper topsoil layer (TABLE 2 | Examples of field trials with economically valuable perennial and woody crops (miscanthus, poplar and willow).
Plant Species/Cultivars/Clones/Hybrids Site Duration TE concentration in soil (mg kg−1) Main results Suggested uses for plants References
Miscanthus M. sinensis Tailing dam (China) n.p. As (418.7), Cd (8.01), Cr (85.1), Cu (15.6), − TE under the normal range for terrestrial plants (except for As) n.p. Zhu et al. (2010)
Moreira et al.
(Miscanthus spp.) Zn (92.5), Ni (43.5), Pb (15.1) − ↑ As concentration in roots (98% of total As concentration in plants)
− TF < 1
− BCF 1 for Pb and Cr
− TF < 1 for Zn, Fe, Mn and Cu
Miscanthus sp. Site near a former Pb and Zn smelter (France) 3 years Zn (334.3), Pb (219.5), Cd (4.5), Cu (20.6) − Soil EDTA-extractable TE ranked as follows: Pb > Cd > Cu > Zn n.p. Iqbal et al. (2013)
− ↓ Cu and Pb soil bioavailability when compared to the reference soil
cultivated with an annual crop
− ↑ Soil organic C in the 20–50 and 200–2000 μm soil fractions
− TE soil availability was correlated with TE and carbon localizations in soil
fractions
M. x giganteus 2 sites in the vicinity of a former smelter processing 3 years Pb (802/683), Cd (26/13.5), Zn (242/147), − ↓ Cd and Pb concentration in aboveground tissues Thermal energy biofuel Barbu et al. (2013)
sulphidic ores (Romania) Cu (224/213) − Good combustions properties of biomass (low ash content and no sulfur
present)
M. x giganteus Contaminated agricultural soil near a former Pb-Zn-Cd ore 6 years Pb (547), Cd (20.8), Zn (2175) − Potential production of 30 tonnes of biomass ha−1 Biomass for energy Pogrzeba et al. (2013)
mining and processing plant (Poland) − ↑ TE concentration in aboveground parts
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− ↓ TE in biomass over the experimental period
− Total TE content in aboveground tissues: 2.2–4.8 kg ha−1 for Pb, 0.055
to 0.12 kg ha−1 for Cd and 9 to 13 kg ha−1 for Zn
M. x giganteus Agricultural contaminated site (France) 8 months Cd (3.6/8.8), Pb (226.4/486.3), Zn (301.2/ − Similar shoot yields to those of plants grown in uncontaminated soil (US) Biomass for thermochemical Nsanganwimana et al.
511.8) − ↑ Cd and Zn concentrations in all organs than those of plants grown conversion (2016)
in US
− ↑ Pb and Zn concentrations in leaves than in stems
− ↓ Soil bioavailable Pb concentration
− TE concentrations depended on element, organ and growth phase
− Nutrient concentration ranked as follows: K > N > P ≥ Ca > Mg > Na
− ↑ Nutrient concentration (except Na) in leaves than in stems at the
maximum DW
Miscanthus hybrids (M. sinensis x sacchariflorus ′GNT41′ and Arable land contaminated by smelting activities (Poland) 2 years Pb (690), Cd (27), Zn (3,028) − ↑ Biomass of all miscanthus (13–16 tonnes ha−1 y−1) Biomass for energy Rusinowski et al.
10
′GNT34′); M.xg − ↓ Shoot height of miscanthus hybrids when compared to M.xg (2019)
− ↑ Leaf Area Index and stem number of miscanthus hybrids
− ↓ Shoot Pb and Cd concentrations of miscanthus hybrids when
compared to M.xg
− ↑ Water-conserving behavior of miscanthus hybrids
Poplar P. trichocarpa × deltoides Alluvial soil polluted by river sediments (new plantation) 7 years Cd (4.4/9.4), Zn (272/986), Cu (25/1,219), − ↓ Growth rate n.p. Lettens et al. (2011)
(Populus spp.) and polluted dredged sediment soil (old plantation) Mn (510) − ↓ Transpiration rate
(Belgium) − ↓ Cd, Zn and Mn foliar concentrations over time in the new plantation
− ↑ TE concentration in leaves
− ↑ Cu concentration in leaves
− No changes in Cd, Zn and Mn foliar concentrations over time in the old
plantation
P. deltoides x (P. trichocarpa x deltoides) (′Grimminge′); P. Former maize field near a metal smelter (Belgium) 2.5 years Zn (343), Cd (5.7), Cu (35), Pb (185), − ↓ Poplar biomass Biomass for energy Ruttens et al. (2011)
trichocarpa x P. deltoides (′Hoogvorst′); P. deltoides x P. nigra − ↑ Plant TE concentrations
(′Muur′) − Chlorosis of leaves observed in some clones
− No change in soil TE concentrations (either total or available)
P. euroamericana (hybrids); P. trichocarpa Sites near Zn and Pb smelters (France) and near a Zn > 18 years Cd (0.8–69), Cu (17–94), Pb (110–3,500), − ↓ Pb uptake Biomass for energy Evangelou et al.
smelter (Germany) Zn (540–11,400) − ↑ Zn and Cd concentrations in leaves (2012b)
− ↓ Cu and C concentration in bark and wood
− ↑ Ca and K concentration in bark and wood
P. nigra x P. maximowiczii; P. nigra Area of former waste incineration plant (Czech Republic) 2 years Cd (0.53–1.3), Zn (96.1–174), Cu − Regular growth and no visuals symptoms of toxicity n.p. Kacálková et al. (2015)
(24.4–80.8) − Cd and Zn concentration ranked as follows: Leaves > twigs > roots
− Cu concentration ranked as follows: twigs > leaves > roots
− BCF > 1 for Cd and Zn in leaves (in general)
− BCF < 1 for Cu in leaves
14 genotypes, e.g.: P. trichocarpa x P. maximowiczii (′Skado′, Soil formerly irrigated with raw wastewaters (France) 4–5 years Pb (74.7–484), Cd (1.98–4.44), Zn − ↑ variability in TE concentration in leaves among genotypes n.p. Pottier et al. (2015)
‘Bakan’); deltoides x nigra (′Vesten′, etc); P. trichocarpa (314–692), Cu (69–218), − TE concentration in leaves ranked as follows: Mg > Zn > Mn Fe > Cu
(′Trichobel′, etc) > Cd
− ↓ Fe and Cu mean concentrations at the beginning of leaf development,
remaining constant until leaf abscission
− Steady increase of Mn, Cd and Zn from leaf emergence until the end of
the summer, and damped just before abscission
− ↓ Mg concentrations just before leaf abscission
− Fe, Mn, Zn and Cd were not remobilized during leaf senescence in any
genotype
Farmland near a former Zn-smelter (Belgium) 3 years Cd (4.1–8.4), Zn (234–488) Variable biomass between clones Biomass for conversion Thijs et al. (2018)
(Continued on following page)
Phytomanagement of Metal(loid)-Contaminated Soils
August 2021 | Volume 9 | Article 661423TABLE 2 | (Continued) Examples of field trials with economically valuable perennial and woody crops (miscanthus, poplar and willow).
Frontiers in Environmental Science | www.frontiersin.org
Moreira et al.
Plant Species/Cultivars/Clones/Hybrids Site Duration TE concentration in soil (mg kg−1) Main results Suggested uses for plants References
e.g.: P. trichocarpa clones; P. trichocarpa x trichocarpa; P. − ↓ Biomass productivity (< 6 tonnes ha−1 y−1)
trichocarpa x P. maximowiczii − Variable biomass and TE accumulation over the years
− Variable Zn and Cd concentrations between poplar clones
Populus deltoides x P. nigra (′Orion′) Area formerly used to electronic waste disposal (Italy) 4 years Cd (0.8), Cu (64.5), Ni (26.8), Pb (75), − TE concentration differed between bark and wood n.p. Nissim et al. (2019)
Zn (286) − ↑ Zn accumulation in the largest poplar plants (60 mm DBH)
− ↑ Cd, Cu and Ni accumulation in slightly smaller plants (50 mm DBH)
− ↑ Pb accumulation in smaller plants (40 mm DBH)
14 genotypes; ex.: P. trichocarpa x P. maximowiczii (′Skado′, Area formerly irrigated with raw wastewaters (France) 4, 7, 10 Pb (74.7–484), Cd (1.98–4.44), Zn − ↑ Biomass of P. ′Vesten′ Biomass for energy Chalot et al. (2020)
′Bakan′); P. deltoides x P. nigra (′Vesten′, etc); P. trichocarpa years (314–692), Cu (69–218), − ↑ Variability in TE concentration among genotypes
(′Trichobel′, etc) − ↓ Soil TE (Cd, Cu and Zn) concentration after 10 years of poplar growth
− No change or increase of macronutrients concentrations after 10 years
of poplar growth
− ↑ TE accumulation in bark
− ↑ TE accumulation in branches, namely Cd, Cu and Zn than in wood
Willow (Salix spp.) S. fragilis (′Belgisch Rood′); S. viminalis (′Jorunn′); S. viminalis x Former maize field near a metal smelter (Belgium) 2.5 years Zn (343), Cd (5.7), Cu (35), Pb (185) − Moderate biomass production n.p. Ruttens et al. (2011)
viminalis (′Christina′) − ↑ Plant TE concentration
− No changes in soil TE concentration (either total or available)
− Chlorosis of leaves observed in some cv.
S. caprea; S. alba Sites near Zn and Pb smelters (France) and 1 near a Zn > 18 years Cd (0.8–69), Cu (17–94), Pb (110–3,500), − ↓ Pb uptake n.p. Evangelou et al.
smelter (Germany) Zn (540–11,400) − ↑ Zn and Cd concentrations in leaves (2012b)
− ↓ Cu and C concentration in bark and wood
− ↑ Ca and K concentration in bark and wood
e.g., S. alba ′Alba′; S. viminalis; S. dasyclados; S. schwerinii x S. Area contaminated by former smelter activities (Belgium) 4 years Cd (6.5), Zn (377) − ↑ Productivity during the first SR cycle (3.7 tonnes DW ha−1 y−1) Biomass for energy Van Slycken et al.
viminalis) − Potential removal of 72 g Cd and 2.0 kg Zn ha−1 (2013a)
− ↑ Removal of Cd and Zn when leaves are included in the harvest
S. x smithiana, S. rubens Area of former waste incineration plant (Czech Republic) 2 years Cd (0.53–1.3), Zn (96.1–174), Cu − Regular growth and no visuals symptoms of toxicity n.p. Kacálková et al. (2015)
(24.4–80.8) − ↑ Cd and Zn in leaves
− No differences in Cd and Zn accumulation between species
− BCF > 1 for Cd and Zn in leaves (in general)
− BCF < 1 for Cu
S. triandra x S. viminalis (′Inger′) Former industrial landfill area (Sweden) 3 years Cu (28–240), Pb (22–1,000), Zn (72–530) − good growth, with yields in line with the expected productivity in Biomass for energy Enell et al. (2016)
commercial applications
11
− ↓ Pb and Cu accumulation in leaves and twigs
− ↑ Soil organic matter content
− No significant differences in soil TE concentrations before and after
willow cultivation (except for Pb in one plot, where a decrease was found)
− ↑ Ecological conditions for nematodes
− ↓ TE concentration in porewater during cultivation
S. purpurea (′Fish Creek′); Salix x dasyclados (′SV1′); Salix Military landfill (Canada) 3 years NH4NO3-extractable TE: As (1.16), Cd − TE (except Cd and Zn) had a significant impact on biomass production n.p. Courchesne et al.
miyabeana (′SX67′) (0.56), Cu (59), Ni (8.8), Pb (21), Zn (89) − Low to moderate biomass production at the third year (2017)
− TE in the whole plant ranked as follows: Zn > Cu > Cd > Ni, Pb > As
− ↑ Zn and Cd concentration in leaves
− ↑ Cu and Pb concentration in roots
− General differences of TE contents in leaves among cv.
− Stable TE concentration over time in shoots and leaves
e.g., S. alba; S. alba x alba; S. viminalis; S. viminalis x S. viminalis Farmland near a former Zn-smelter (Belgium) 8 years Cd (4.1–8.4), Zn (234–488) − Variable biomass between clones Biomass conversion Thijs et al. (2018)
Phytomanagement of Metal(loid)-Contaminated Soils
− Variable biomass and TE accumulation over the years
− ↓ Biomass productivity (< 6 tonnes ha−1 y−1)
− ↑ Extraction of Cd and Zn of some clones
S. viminalis Urban area (France) 3 years Cd (1.66), Zn (617) − Zn and Cd soil biavailability was maintained over the 3 years Green chemistry to produce Grignet et al. (2020)
− Regular growth of willows, with good health status Zn-ecocatalysts
− ↑ Survival rate
August 2021 | Volume 9 | Article 661423
− ↑ Foliar concentration of Zn and Cd in leaves
− BCF > 1 for Cd and Zn in leaves
Abbreviations are as follows: n.p., not provided; TF, Translocation factor; BCF, Bioconcentration factor; BAF, Bioaccumulation factor; DW, dry weight; cv., cultivar; ↑, high/higher/increase; ↓, low/lower/decrease; DBH, diameter at breast
height; SR, shot rotation.
Values for TE concentrations are given for the upper topsoil layer (Moreira et al. Phytomanagement of Metal(loid)-Contaminated Soils
and medicinal purposes (Bashir et al., 2015). Sunflower can varieties and cultivars of maize are widely cultivated across the
also be used to produce hydrogen fuel (Antonopoulou et al., globe for food or livestock forage (Wuana and Okieimen, 2010).
2016). However, other valuable economic products can be obtained
Besides these established industrial, commercial and from maize such as bioethanol (Meers et al., 2010), biogas
medicinal applications, its high yields, TE-tolerance and (Thewys et al., 2010; Van Slycken et al., 2013a - Table 1),
capacity to generate a cluster of biomass-based products digestate for soil conditioning (from which TE can also be
support the great potential of sunflower as an attractive crop recovered) (Meers et al., 2010; Table 1), biomass for
for phytomanagement. Also, the low TE contents usually production of electrical and thermal energy (Schreurs et al.,
present in the seeds and oil from sunflower plants grown in 2011; Witters et al., 2012a,b; Van Slycken et al., 2013a; Cheng
contaminated areas points out to a limited risk of contaminating et al., 2015; Rizwan et al., 2017), sweeteners (Ranum et al., 2014),
the food chain (Angelova et al., 2016; Mench et al., 2018), and and starch for food and industrial applications (De Vasconcelos
fosters their use for, e.g., feeding livestock (Mench et al., 2018). et al., 2013). Maize can also be used for the production of
Several sunflower cultivars show tolerance to As (Piracha et al., charcoal/biochar (Břendová et al., 2015).
2019), Cd (Thijs et al., 2018; Zehra et al., 2020a; Table 1), Cu Maize has been reported to be tolerant to several TE, e.g., Cd
(Kolbas et al., 2011, 2014; Mench et al., 2018), Cr (Aslam et al., (Van Slycken et al., 2013a; Xu et al., 2013; Kacálková et al., 2014 -
2014), Ni (Ahmad et al., 2011), Pb (Kacálková et al., 2014; Zehra Table 1; Moreira et al., 2014; Rizwan et al., 2016), Cu (Jarausch-
et al., 2020b; Table 1), Zn (Herzig et al., 2014; Marques et al., Wehrheim et al., 1996; Karczewska et al., 2009), Zn (Moreira
2013), U (Kötschau et al., 2014 - Table 1; Meng et al., 2018), Cs et al., 2016a,b; Van Slycken et al., 2013a - Table 1), Pb (Cheng
and Sr (Brooks, 1998). They are also able to successfully grow in et al., 2015; Table 1), and Cr and Ni (Kacálková et al., 2014;
multi-metal(loid) contaminated areas, as is the case of mining Table 1). In fact, maize is usually recognized as a root TE
(Kötschau et al., 2014; Table 1), industrial (Herzig et al., 2014; accumulator (Li et al., 2009; Meers et al., 2005). However, this
Mench et al., 2018) and agricultural sites (Thijs et al., 2018; root-accumulating phenotype largely depends on soil properties
Table 1). Regardless of their tolerance, sunflowers’ response to and genetic variability. Its capacity to withstand high TE levels in
bioavailable TE excess can be highly variable among cultivars, soil (Wuana and Okieiman, 2010) coupled with its potential for
with some showing higher TE extraction efficiency the generation of biomass-based products, makes maize an
(Nehnevajova et al., 2005), which can limit crop yield. interesting annual crop for phytomanagement. Kernels tend to
Therefore, efforts have been made to implement breeding have a lower TE content than stems and roots (Putwattana et al.,
programs aimed at developing new cultivars/hybrids with 2015; Wang et al., 2016; Xu et al., 2013 - Table 1), making them
increased TE-tolerance. For instance, Cd and Zn potentially suitable for animal feeding if legal TE thresholds are
concentrations contrasted by a factor of ≈2 in 14 sunflower not surpassed (Meers et al., 2010; Van Slycken et al., 2013a; Cheng
cultivars grown in spiked solutions, with differences being et al., 2015; Table 1). Maize cultivars (e.g., Bright Jean Number 7)
mainly due to uptake and translocation patterns (Laporte et al., have been bred in the past decades to cope with rising
2015). Likewise, attempts to develop variants with increased temperatures and low water supply (Cheng et al., 2015;
drought and salt tolerance have been performed (Kane et al., Table 1). Nonetheless, the use of maize for phytomanagement
2013), as these abiotic stressors are frequently found in TE- remains a challenge under the current climate change scenario,
contaminated soils. Sunflower variants with high TE especially in dry areas, since it can imply higher costs to
extraction/stabilization capacity can be obtained by stakeholders due to its water requirements or lower yields in
chemical mutagenesis (EMS–ethyl-methane-sulfonate), with arid or semi-arid areas (Meers et al., 2010). High biomass
some of them being more effective in phytoextracting TE (Cd, producing cultivars have been developed (Meers et al., 2005)
Cu, Pb and Zn) in field trials, compared to their mother lines to meet the need for renewable energy sources. These high
(Herzig et al., 2014; Kolbas et al., 2011; 2018; 2020). These biomass cultivars are most adequate for biomass production in
variants also showed a higher activity of antioxidant enzymes polluted areas, while mitigating the risk of the spread of
(Nehnevajova et al., 2012). In any event, cropping systems are contaminants to other environmental compartments. For
critical drivers of sunflower performance (Kolbas et al., 2011; instance, maize grown in a heavily Pb-contaminated area
Rizwan et al., 2016; Mench et al., 2018). For instance, crop (6,000 mg kg−1) in Taiwan could produce about
rotation can reduce allelopathy and the spread of fungal ≈1545 GJ ha−1 y−1 of thermal energy or the combination of
diseases (Markell et al., 2015). Selected sunflower field trials 25 tons of grain for livestock feeding plus the production of
are described in Table 1. 1172 GJ ha−1 y−1 of thermal energy from the remain plant
parts (Cheng et al., 2015). Meers et al. (2010) estimated that
Maize (Zea mays L.) as much as around 119 to 166 GJ ha−1 y−1 of electrical and
Maize is an edible annual plant of the Poaceae family native to thermal energy could be generated from maize grown in a site
southwestern Mexico, where it was domesticated from Balsas contaminated with Cd, Zn, and Pb in Flanders (Belgium). This
Teosinte (Van Heerwaarden et al., 2011). Maize plants prefer approach can reduce the emission of CO2 by 21 tons ha−1 y−1,
fertile, well-drained and moisty soils, and are sensitive to frost, when compared to the use of fossil fuel to generate the same
water logging and drought (Wuana and Okieimen, 2010). These amount of energy. Moderately contaminated agricultural areas
liabilities, alongside the high water demand, pose limitations for could also be used to grow energy maize instead of fodder maize,
the use of this crop to recover contaminated areas. Several without loss of income to farmers (Meers et al., 2010; Van Slycken
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